1. Evolutionary Biology
  2. Neuroscience
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Tachykinin signaling inhibits task-specific behavioral responsiveness in honeybee workers

  1. Bin Han
  2. Qiaohong Wei
  3. Fan Wu
  4. Han Hu
  5. Chuan Ma
  6. Lifeng Meng
  7. Xufeng Zhang
  8. Mao Feng
  9. Yu Fang
  10. Olav Rueppell  Is a corresponding author
  11. Jianke li
  1. Chinese Academy of Agricultural Science, China
  2. University of Alberta, Canada
Research Article
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Cite this article as: eLife 2021;10:e64830 doi: 10.7554/eLife.64830

Abstract

Behavioral specialization is key to the success of social insects and leads to division of labor among colony members. Response thresholds to task-specific stimuli are thought to proximally regulate behavioral specialization but their neurobiological regulation is complex and not well-understood. Here, we show that response thresholds to task-relevant stimuli correspond to the specialization of three behavioral phenotypes of honeybee workers in the well-studied and important Apis mellifera and Apis cerana. Quantitative neuropeptidome comparisons suggest two tachykinin-related peptides (TRP2 and TRP3) as candidates for the modification of these response thresholds. Based on our characterization of their receptor binding and downstream signaling, we confirm a functional role of tachykinin signaling in regulating specific responsiveness of honeybee workers: TRP2 injection and RNAi-mediated downregulation cause consistent, opposite effects on responsiveness to task-specific stimuli of each behaviorally specialized phenotype but not to stimuli that are unrelated to their tasks. Thus, our study demonstrates that TRP-signaling regulates the degree of task-specific responsiveness of specialized honeybee workers and may control the context-specificity of behavior in animals more generally.

Data availability

Original data have been deposited to ProteomeXchange Consortium with the dataset identifier PXD018713 under http://proteomecentral.proteomexchange.org or are provided as supplementary data files.

The following data sets were generated

Article and author information

Author details

  1. Bin Han

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6974-8699

  2. Qiaohong Wei

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  3. Fan Wu

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7923-3808

  4. Han Hu

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  5. Chuan Ma

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  6. Lifeng Meng

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  7. Xufeng Zhang

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  8. Mao Feng

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  9. Yu Fang

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

  10. Olav Rueppell

    Biological Sciences, University of Alberta, Edmonton, Canada
    For correspondence
    olav@ualberta.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5370-4229

  11. Jianke li

    Chinese Academy of Agricultural Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Natural Science Foundation of China (31970428)

  • Bin Han

Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2015-IAR)

  • Jianke li

National Project for Upgrading the Beekeeping Industry of China

  • Jianke li

Modern Agro-Industry Technology Research System (CARS-44)

  • Jianke li

University of North Carolina at Greensboro

  • Olav Rueppell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Publication history

  1. Received: November 12, 2020
  2. Accepted: March 23, 2021
  3. Accepted Manuscript published: March 24, 2021 (version 1)
  4. Version of Record published: March 31, 2021 (version 2)

Copyright

© 2021, Han et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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